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Current Concepts Review - Limb-Lengthening, Skeletal Reconstruction, and Bone Transport with the Ilizarov Method*

Investigation performed at the University of Arkansas for Medical Sciences, Little Rock

	Introduction

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Ilizarov embarked on his remarkable medical career as a general practitioner in the small industrial town of Kurgan, Siberia, after World War II^69,75,96. Antibiotics were scarce, and chronic osteomyelitis associated with loss of bone, non-unions, and skeletal deformities were so common that Ilizarov found himself practicing orthopaedics although he had had no formal training in that specialty. With the use of modular-ring external fixators and transosseous wires attached to the rings under tension to stabilize the bone fragments, he introduced the concept of induction of local bone formation with a minimally invasive procedure^69,75,96. Ilizarov coined the term distraction osteogenesis to describe the induction of new-bone formation between osseous surfaces that are gradually pulled apart⁹. His clinical successes in the salvage of limbs that would otherwise have been amputated and in the return of disabled patients to productive levels of activity eventually spread by word of mouth throughout the Communist bloc of countries^69,75. By 1981, a group of Italian orthopaedic surgeons had learned of his technique⁹. More recently, the method was introduced in North America, where it has been adopted primarily for limb-lengthening^{12,49,120,125} and the correction of limb deformities as well as the treatment of non-unions and bone loss secondary to trauma, infection, or tumor^{39,41,43,46,76,78,99,114,124,135,142}.

Ilizarov practiced in an isolated area of the world without access to the many technological and medical advances that took place during the four decades after World War II. As a result, he relied on distraction osteogenesis to treat a variety of musculoskeletal conditions. The reconstruction of bones affected by post-traumatic conditions, such as intercalary defects, shortening, and deformity, was the broadest application of his method. Bone transport, which involves the transport of a bone fragment across an intercalary bone defect with new-bone formation at the trailing end¹⁸, was used to salvage many limbs that otherwise would have been amputated because of non-union, osteomyelitis, or extensive segmental bone loss^{10,18,24,35,39,41,43,46,70,76,78,99,114,124,135,142,157,163}. Ilizarov later tried to use this method for limb-lengthening, expanding the indications to adult patients, the upper extremity, and anatomical discrepancies of more than 15 per cent of the bone—that is, in excess of the amount of lengthening that was conventionally accepted at that time. In addition, he attempted to treat short limbs associated with conditions such as dwarfism. Although the method initially enjoyed wide popularity and interest in the United States, its complex and tedious nature¹²⁵ and the frequency of complications^52,127 combined with overzealous claims of success prompted appropriate skepticism.

	History

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In order to appreciate the contributions of Ilizarov to the field of orthopaedic surgery, it is important to relate his achievements to events that preceded them historically^120,136. Three concepts—limb-lengthening, external fixation, and regeneration of bone—can be traced to earlier orthopaedic investigators.

As far as we know, the first successful lengthening of deformed limbs was reported by Codivilla⁴⁷, who, in 1905, described the use of an osteotomy of the cortex and immediate application of traction force to a calcaneal pin, with or without the use of narcotics. In 1908, Magnuson¹¹¹ studied the potential for spontaneous bone-healing in an experimental study involving sixteen dogs and, in 1913, presented three clinical case reports. In the canine studies, only four procedures involving acute lengthening at the site of a step-cut osteotomy were considered entirely successful. Complications, including breakdown of the wound, fracture, and infection, resulted in the death of or the need to kill eight of the dogs before completion of the study. Magnuson reported successful femoral lengthening of two to three inches (five to eight centimeters) in the human patients.

To the best of our knowledge, Ombredanne¹²³ was the first to use an external fixator for limb-lengthening. In 1913, he reported lengthening of bone at a rate of five millimeters per day after the production of an oblique osteotomy of the femur; however, skin necrosis and infection occurred. In 1921, Putti¹⁴³ slowed the rate of distraction to two to three millimeters per day with a monolateral fixator and half-pins.

The idea of a latency period to promote the formation of bone was introduced by Abbott¹ in 1927. Abbott performed a step-cut osteotomy, with preservation of the periosteum, and then allowed a seven-to-ten-day latency period before applying distraction through a spring-loaded, force-controlled device. Fifteen years later, Brockway and Fowler³⁰ reported the long-term results of 105 lengthening procedures that had been done with the Abbott technique. With use of a five-day latency period and a rate of distraction of one to 1.5 millimeters per day, five centimeters of lengthening required one to two years of treatment (including time for distraction and healing), or approximately three to four months per centimeter. In 1936, Anderson⁶ reported several innovations for femoral lengthening, including the use of wires attached to the apparatus under tension and a technique for percutaneous osteotomy. Bost and Larsen²⁹ modified the technique further by performing femoral lengthening over an intramedullary rod after creation of an osteotomy with a power or Gigli saw. Although some femora united spontaneously, delayed union was frequent.

The understanding of the basic science of bone-lengthening, particularly as it relates to the effects on the periosteum and the growth plate, was clarified during the 1950s and the 1960s. Experimental work by Kawamura et al.¹⁰² demonstrated that the periosteum sustained less damage if it was stripped as a tube circumferentially and that peripheral blood flow diminished as the rate of lengthening increased. In 1958, Ring¹⁴⁵ distracted growth plates, observing that they fractured but that the periosteal tube remained intact and gave rise to a shell of new bone. The first reported transphyseal lengthening with use of an Ilizarov ring fixator in the United States followed eighteen years later⁶⁴.

From 1970 to 1990, the Wagner method of lengthening¹⁶⁸ became more popular than the Anderson technique among most pediatric orthopaedists. This method involves use of a monolateral fixator that allows the patient to get out of bed; a three-stage plan is used to expedite treatment. The concept introduced by Wagner involves cutting of the periosteum, fascia, and other constraining tissues in order to minimize resistance; limiting the lengthening to a maximum of seven centimeters; relatively rapid distraction (as much as two millimeters per day) as tolerated by the patient, who is awake; and bone-grafting of the defect after the intended amount of distraction is achieved. The mid-diaphyseal osteotomy is made with an oscillating saw, and a specially designed internal fixation plate replaces the external fixator after lengthening has been achieved.

	Technical Considerations

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Because the Ilizarov technique is used to treat some of the most challenging conditions in orthopaedics, including those following previous failed orthopaedic treatment, preoperative planning can be complex. The method requires analysis of one or more sites of deformity and deficiency of bone or soft tissue, or both. Mechanical and anatomical axes^130-132 are identified, and a plan is formulated that includes a strategy for managing the biological and mechanical requirements at each site⁸⁷. Multiple transosseous wires or half-pins must be inserted through so-called safe zones within the limb. Extensive preoperative education of the patient and the family facilitates compliance with the lengthy and often painful treatment. The risks and the need for extensive postoperative treatment (which involves frequent clinical visits, mechanical adjustments, care of the pin sites, incremental lengthening, and exercise) must be understood. The operation is usually followed by a brief stay in the hospital, a latency period (the period after a corticotomy and before distraction is initiated when, as a result of a normal osteotomy or fracture-healing, the cut bone surfaces are bridged with callus), a distraction period, and a consolidation period. The total duration of treatment divided by the number of centimeters of new-bone formation, usually one month per centimeter of new bone formed in children and two to three months per centimeter of new bone in adults¹², is referred to as the healing index.

Distraction osteogenesis refers to the production of new bone between vascular bone surfaces created by an osteotomy and separated by gradual distraction⁹. Distraction physiolysis refers to the mechanical distraction of the growth plate without an osteotomy but with a physeal fracture^{6,64,118,125,145}. Although Ilizarov used this technique initially^93,95,96,125, he later preferred a metaphyseal site for the osteotomy and distraction in order to avoid growth arrest¹²⁵. The largest reported series of distraction physiolyses demonstrated excellent bone formation by intramembranous ossification¹¹⁸. Most pediatric orthopaedists avoid distraction physiolysis because it can cause sudden, intense pain at the site of the fracture as well as growth arrest^37,118,141.

With regard to spontaneous bone formation, the metaphyseal site has been shown to offer several advantages compared with other sites. These include greater blood flow, better collateral circulation, greater trabecular surface area, a thin cortex that facilitates separation with a chisel, and greater inherent stability^17,65,93-96. Bone formation by distraction osteogenesis may be inhibited in the diaphysis because blood at this site is supplied by a single nutrient artery¹¹. When distraction must be performed in the diaphysis, preservation of the periosteum is of particular importance because it contains its own blood supply¹⁰².

Ilizarov introduced the concept of the corticotomy as a procedure distinct from routine osteotomy. This term is used throughout the remainder of this review to identify this specific technique. Ilizarov defined corticotomy as a low-energy osteotomy of the cortex, with preservation of the local blood supply to both the periosteum and the medullary canal^93,94,149. He believed that it enhanced bone formation. Other surgeons and investigators have found the corticotomy not only difficult to perform and unreliable with regard to maintaining the medullary circulation but also unnecessary for satisfactory osteogenesis^{2,32,54,65,129,140,178}. The evolution and technique of Ilizarov's corticotomy have been well described¹⁴⁹. Ilizarov's method of maintaining vascularity of all of the bone surfaces by cracking only the cortex, although difficult to master, clearly provides the greatest bone mass and volume within the distraction gap^{9,11,12,17,19,20}. Nonetheless, disruption of the medullary canal with a Gigli saw¹²⁹ or an oscillating saw^56,65,168, simple pre-drilling with subsequent manual osteoclasis (the DeBastiani method^17,44), or even intramedullary reaming and nailing³² can result in bridging of a distraction gap with bone if the periosteal tube is maintained.

Many authors^{9,11,12,17,19,20,32,54,177,178} have indicated that the periosteum is the major contributor to osteogenesis during distraction. As previously noted, this contribution is probably a reflection of the importance of the periosteum in providing vascularity. Consequently, methods of bone separation that disrupt the periosteum, such as widely displaced corticotomies or osteotomies, can result in decreased osteogenesis⁶⁵. Nonetheless, any vascularized bone surface, whether periosteal, endosteal, cortical, or trabecular, can promote osteogenesis when it is gradually distracted from a similarly vital vascular surface^9,11,12,20. For example, a partial defect resulting from cavitary osteomyelitis can be bridged by transport of a small fragment of adjacent cortex, and massive loss of tibial bone can be treated with transverse fibular transport after a longitudinal corticotomy^10,18,96.

Although Ilizarov often attributed special biological effects and enhanced healing to the use of the ring external fixator with wires attached under tension, distraction osteogenesis and bone transport can be successfully accomplished with use of a monolateral, half-pin frame^{19,21,36,51,56} or even intramedullary nails inserted after reaming³². Ilizarov emphasized that stability of the frame as provided by his fixator is extremely important for successful bone-healing. However, while most modern monolateral fixators are sufficiently stable to distract a corticotomy site, maintain a gap, and protect the biological elements that bridge the gap, they are limited by an inherent cantilever design that imparts eccentric loads on the bone and may result in undesirable angulation of the lengthened segment^14,19. The choice of external fixator is now generally determined by the experience and preference of the surgeon, the complexity of the problem, and the number of sites that need treatment^14,141,147. As a general rule, monolateral fixators may not be as well suited as ring fixators for the mechanical correction of deformities with angulation or rotation or those that need more than two sites of treatment.

Each type of external fixator exhibits individual mechanical characteristics that may affect osteogenesis and healing^{14,34,62,82,104,133,138,156}. The stiffness and stability of a fixator system are dependent on many variables, including the diameter of the wires, the number of wires used, and the tension on each wire^8,34. In addition, the configuration of the wires—that is, the angles that they make with respect to each other and the space between them—affects the fixator system^14,34. The stiffness and stability of the system are also affected by the diameter of the rings, the number of rings used, and the spacing between the rings^{14,34,104,133,138}. Gross instability of the frame can lead to two completely divergent outcomes: premature consolidation, if the fixation is too loose to distract the corticotomy site, or non-union, if macromotion disrupts the delicate osteogenic bridge. Consequently, an unstable construct should not be used^{9,12,20,21,62,82}.

The most versatile system seems to be the ring fixator with half-pin modifications^{62,73,77,83,118,121,128,171}. It can transmit gradual mechanical forces and movements of bone in any plane (frontal, sagittal, or transverse) or direction (axial, angular, translational, rotational, or any combination) at an unlimited number of treatment sites, and it has the potential to cross and protect active joints^{14,53,70,87,88,90,109,117}. Wires attached to the frame under tension, which can achieve stiffnesses equivalent to those of the much-larger-diameter half-pins, exhibit unique self-tensioning effects that may facilitate load-sharing with the supported bone either in distraction or in compression modes^8,15. As the use of half-pins results in half the number of sites of soft-tissue transfixion, they can decrease the number of pin-related and soft-tissue complications^52,73,74,77 and can potentially improve the comfort of the patient and the tolerance to treatment.

It is generally agreed that some period of latency subsequent to a corticotomy enhances the formation of bone^{12,17,67,173,174,178}. The duration of the latency period in most clinical reports^{12,28,37,51,63,103,125,141,174} has ranged from three to ten days, with the shorter periods used with the classic Ilizarov corticotomy at metaphyseal locations and the longer periods needed for more traditional osteotomy techniques performed with an oscillating saw, especially in diaphyseal bone. Experimentally, the limits of these periods have been tested further; good bone formation was seen in canine tibiae after no latency period, and the risk of premature consolidation of the gap increased with latency periods of fourteen to twenty-one days¹⁷.

The rate of distraction can vary, depending on multiple factors. Ilizarov employed a distraction rate of one millimeter per day to facilitate bone formation⁹⁴. The rate may need to be decreased in situations in which the host-bone surfaces are less vascular, such as in dense cortical bone. Indeed, experimental studies have demonstrated that rates ranging from 0.5 to two millimeters per day have reliably led to bone formation after a metaphyseal corticotomy, but more than two millimeters per day may exceed the potential for vascular ingrowth at a diaphyseal site^11,66. In general, bone may form more slowly in adults and necessitate slower rates of distraction, whereas children may benefit from rates of more than one millimeter per day in order to avoid premature consolidation of the gap, especially at sites of metaphyseal lengthening. Angular lengthening requires special consideration^{9,12,13,19,87,101,178}. The physician must choose a rate of distraction that avoids premature consolidation at the apex but does not exceed the potential for ingrowth of the vascular supply at the base of the opening wedge at the lengthening site. The effect of distraction on soft tissues must also be taken into account. A rate of one millimeter per day may be too rapid for the growth of certain soft tissues, such as muscle^{102,108,116,154,177}, although it seems adequate for nerves^{31,97,107,112,153,158}.

The rate of distraction is usually divided into a daily incremental rhythm of four times a day^{12,24,63,103,125}. Patients have less pain and bone formation seems more reliable with this method than with once-a-day methods^51,52. Ilizarov introduced a motorized system for quasi-continuous distraction, which divided the rate into sixty increments, and claimed that bone formation appeared to be an example of true tissue regeneration⁹⁴. However, clinical and experimental results with similar motorized systems have not yet justified the extra expense, time, and bulk of the system.

The Ilizarov method, as originally described for lengthening, treatment of non-union, and bone transport, does not involve the use of bone-grafting^95,96. More recent experience has demonstrated that autogenous bone graft enhances healing and shortens the time to removal of the frame in certain situations. After transport of a bone fragment, bone-grafting of the site of contact between the leading edge of the transported fragment and the host bone may facilitate healing of this area, which is referred to as the docking site^12,76. Bone-grafting may also be necessary in the case of cystic degeneration of the distraction gap¹².

	Experimental Findings

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The Ilizarov method and the model of distraction osteogenesis have been studied extensively. Ilizarov performed most of his experimental work on a canine tibial lengthening model^93,94,96. While some investigators have reproduced this model^{9,11,12,17,19,20,22,45,124}, others have modified it for lengthening of the femur¹²², radius and ulna⁵⁴, or mandible^50,66 and for bone transport^32,56. Studies have been performed on many animals, including dogs^{9,11,12,17,19,20,22,45,170}, sheep^36,55,67, rabbits^{5,106,108,173,174,177,178}, calves⁹⁷, and rats¹⁵². The net product of these investigations has markedly expanded the understanding of the histological, biochemical, radiographic, vascular, and mechanical properties, as well as the soft-tissue effects, of distraction osteogenesis.

Most histological investigations of the Ilizarov method have confirmed that bone forms from pure intramembranous ossification^{9,12,19,20,54,66,93,94,96,101,148,151,164} occurring in uniform zones. A central zone comprised of type-I collagen^101,164 bridges adjacent zones of vascular ingrowth, where proliferating and differentiating osteoblasts deposit osteoid along the collagen bundles (Fig. 1). Each of these expands into zones characterized by longitudinal columns of bone, which reach uniform diameters. All of these zones parallel the distraction force imparted by the external fixator and bridge the surfaces of the host bone as they are distracted apart. The columns of bone are eventually interconnected transversely, forming a honeycomb appearance on microradiographs^13,68,124 and scanning electron microscopy^9,20,68. When distraction is stopped, the gap begins to consolidate. Columns of bone bridge the collagen interface, and rapid bone-remodeling occurs.

View larger version (125K): [in this window] [in a new window]   Fig. 1 High-magnification photomicrograph showing fibroblasts and osteoblasts anchored to collagen fibrils in an area where osteogenesis is occurring as a result of distraction. The osteoblasts are depositing osteoid directly on these collagen fibrils (hematoxylin and eosin, x 60).

Histological variations have been reported, with some studies demonstrating predominantly fibrocartilage in the distraction zone^177,178. However, most studies of animal models have shown that bone is formed by intramembranous ossification, a finding that was also demonstrated in a specimen of human bone formed by distraction osteogenesis¹⁵¹.

Various factors can affect the quality of the bone formation. In certain instances, accumulations of cartilage can lead to non-union^9,12. Instability due to fixator constructs that allow excessive motion between the distracted bone segments^9,12 may lead to local hemorrhage and the formation of islands of cartilage. Local dysvascularity of one or both distracted surfaces can occur secondary to thermal necrosis (for example, from uncooled power tools⁶⁵) or from a high-energy injury such as that resulting from a widely displaced or comminuted osteotomy⁹³. The resultant ischemic tissue may fail to form bone and could result in a fibrous or cartilaginous non-union^9,12,13. Cystic degeneration of the gap can occur and is thought to be related to venous or lymphatic congestion^9,12,13.

Immunohistochemical analysis has provided evidence of active angiogenesis with the identification of two constituents of vascular basement membrane—laminin and type-IV collagen⁶⁶. Histological and ultrastructural studies have localized growth of thin-walled capillaries between the new columns of bone^{9,13,19,20,97} (Fig. 2). Vessels of uniform diameter that extend from each surface (periosteal and endosteal) of the host bone toward but not across the central zone of collagen and are oriented in the same direction as the longitudinal columns of new bone have been demonstrated with microangiography^{9,13,19,20,54}. Regional perfusion studies have demonstrated increased blood flow (of as much as ten times that in controls) at the site of bone formation^9,11,13,124. In addition, increased blood flow has been found at distant sites within the same bone¹¹. These increased perfusion levels do not seem to be prolonged by an increase in the period of distraction^9,11,13, but blood flow in the range of three times that of control levels persists for at least seventeen weeks after corticotomy^9,11,13.

View larger version (120K): [in this window] [in a new window]   Fig. 2 High-magnification photomicrograph showing a column of bone that was formed by distraction osteogenesis as well as two parallel vascular sinusoids of approximately the same diameter (150 micrometers) (aniline blue, x 40).

View larger version (76K): [in this window] [in a new window]   Fig. 3 High-resolution radiograph showing the microcolumns of new bone extending from each cut surface of the proximal aspect of a canine tibia toward the central radiolucent zone (unmineralized collagen matrix) at the time of earliest bridging (end-distraction and early consolidation) (X 1).

The time sequence of radiographic bone formation at metaphyseal compared with diaphyseal sites has been measured experimentally¹⁷. The metaphyseal sites demonstrated bone formation and remodeling earlier, with an over-all bone-healing index of twenty-two days per centimeter of new bone compared with 26.5 days per centimeter at the diaphyseal sites. The rate of linear bone formation ranged from 200 to 400 micrometers per day in these experimental models. This is four to eight times faster than the fastest physeal growth in an adolescent patient (fifty micrometers per day) and is equivalent to that occurring in the fetal femur^9,12,13.

Studies of animals have demonstrated that, in terms of axial^13,170, torsional¹²⁴, and bending¹³ loading, the mechanical stiffness of the newly formed bone, when measured six weeks after removal of the fixator, is approximately 50 per cent that of normal intact bone. The peak tensile loads have been found to increase linearly with time after the lengthening is completed¹⁷⁰.

Methods for the measurement of in vivo load have been refined since they were initially reported for limb-lengthening^1,102. During distraction, in-line strain gauges have been used to measure loads or the force resisting mechanical distraction^{12,13,15,16,173}. Most studies have confirmed that the load increases with time and with increasing mineralization of the gap^12,13,16,139. After each increment of mechanical distraction, the load increases and then decreases slightly to a higher resting baseline level^{32,139,173,176}. Monolateral fixators¹³⁹ and intramedullary rods³² contribute friction, adding to the over-all load. The higher loads measured during distraction physiolysis are believed to be related to the strong resistance of the growth-plate structures¹³⁹. The lower loads measured during bone transport may be associated with soft tissues, which are rearranged rather than lengthened^32,139. A diurnal variation has been found, with larger decreases in peak load during the sleeping hours, perhaps related to muscle relaxation¹⁸⁰.

Equivalent distraction increments in length require different loads depending on the specific bone or even the location within a bone. Nine metaphyseal and eleven diaphyseal distraction sites in canine tibiae were compared at weekly intervals^12,13,16. With a 15 per cent lengthening performed in all twenty animals, the tibiae that were lengthened at the metaphysis had significantly higher loads (mean, 155 newtons) (p < 0.002) than those that were lengthened at the diaphysis (mean, 111 newtons). This was the case despite the use of identical fixation devices, pin placement, and soft-tissue stretching. Peak loads (428 to 673 newtons) during clinical femoral lengthening were much higher than the peak loads, measured with similar strain gauges, reported earlier for tibial lengthening (approximately 200 newtons)¹⁸⁰.

Experimental force measurements³² have localized the load to the site of new-bone formation. These in vivo measurements were made during lengthening of canine tibiae while the fibula and the soft tissues (skin, fascia, muscles, and periosteum) spanning the distraction gap were progressively removed until only the gap tissue remained to bridge the site of distraction^13,84. The resistance remaining in the gap tissue was high, representing more than 70 per cent of the entire load. Furthermore, as the collagen bridge progressively mineralized, the resistance increased^{9,13,16,20,84,173,174}. No difference in the stress measurements was found between the metaphyseal and diaphyseal sites. High stress levels were associated with incomplete corticotomy or premature consolidation^13,16, whereas low stress levels after three weeks of distraction indicated disruption of the osseous bridge and predicted eventual non-union^13,16.

The effects of lengthening on soft tissue adjacent to the distraction site have been studied less extensively. Clinical problems related to muscles are proportional to the amount of lengthening^{7,12,90,100,109,127,165}, which is expressed as a percentage of the preoperative length of the bone. As much as 10 per cent lengthening is well tolerated by muscle^13,108,178, but substantial histopathological changes occur after limb-lengthening of 30 per cent^102,108,116. It was demonstrated, with use of markers on the periosteum and muscle, that the periosteum immediately adjacent to the site of the osteotomy stretched half as much as the gap between the bone ends, so that the bone actually slid under the periosteum, while muscle in the immediate region of distraction stretched only 20 per cent of the gap^103,177. This indicated that the entire muscle, from the origin to the insertion, participated in the elongation process¹⁷⁸. Nerves, arteries, and veins had histological evidence of temporary degenerative changes, but these disappeared two months after the lengthening⁹⁷. Other studies on animals have demonstrated that direct injury to a nerve from penetration with a fixation wire results in loss of somatosensory evoked potentials¹¹² and acutely induced nerve stretch of 15 per cent decreases the motor action potentials³¹. Gradual (one millimeter per day) femoral lengthening of 20 to 40 per cent has been shown to cause complete peroneal palsy¹⁵⁸, while loss of neural function seems to be avoided with nerve stretch of less than 6 per cent¹⁵³. Finally, the risk of neural dysfunction has been shown to be directly proportional to the rate of distraction¹⁰⁷.

During limb-lengthening, the articular cartilage may be subjected to abnormal and even pathological conditions, including altered weight-bearing activities, limited motion of the joint, and abnormally high reactive forces in the joint. The reactive forces in the hip and the knee of a fresh cadaver measured during an acute, gradual femoral lengthening were shown to increase linearly with continued distraction¹²².

Short-term changes in the articular cartilage of the knee have been observed histologically after 30 per cent lengthening of a canine femur¹⁵⁵ and a rabbit tibia¹⁰⁶. After the lengthening, the physeal cartilage in the rabbit model also underwent histopathological changes, including reduced thickness of the hypertrophic and proliferative zones¹⁰⁶; however, changes in the growth rate were not observed after clinical lengthening⁹¹.

	Clinical Applications

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The three areas in which the Ilizarov method has made important contributions are limb-lengthening, the treatment of deformity or non-union, and bone transport.

Limb-Lengthening
The Ilizarov method allows the surgeon to perform complex and extended lengthening of both congenital and acquired short limbs, but the technique can be difficult and time-consuming to master compared with methods that involve use of a monolateral fixator^51,52. The DeBastiani method has gained increasing popularity among pediatric orthopaedists because it is technically less demanding for the surgeon and the monolateral fixator tends to be more comfortable than a circumferential ring fixator for the patient^2,140,141. The DeBastiani method relies on a more conventional osteotomy, which involves operative opening of the periosteum, drilling across both the near and the far cortices in several directions, interconnection of visible drill-holes with an osteotome, and completion of the osteotomy with a manual osteoclasis. Correction of deformity with this method requires manual rotation or angulation performed in the operating room. Before distraction is initiated, a prolonged latency period of about fourteen days is necessary until callus is seen radiographically. However, there is a possibility of subsequent deformity due to incomplete correction or loss of correction by eccentric loads working against the monolateral fixator, and additional manual correction, usually performed with the patient under anesthesia, may therefore be necessary^{2,14,105,140,141}.

The Ilizarov method has advanced limb-lengthening in several ways. First, it is now possible to lengthen limbs at several sites simultaneously as well as to correct deformity. In addition, since the method allows for gradual lengthening with protection of adjacent joints in a frame that permits most activities of daily living, the possibilities of limb-lengthening have been extended. Perhaps most importantly, large skeletal defects can heal without bone-grafting, internal fixation, or multiple operations.

Clinical investigations of the Ilizarov method have confirmed that the rate and quality of bone formation can be influenced by certain factors that are under the control of the physician^125,140. These factors include the amount of lengthening that is attempted, the site of the lengthening, the selection of the bone to be lengthened, and the number of sites of lengthening within the bone. The rate of healing is directly proportional to the length of the distraction gap—the greater the lengthening, the longer the time needed for treatment—and is expressed as the healing index (the number of months of treatment for each centimeter of new bone)^2,63. Other factors affect the rate of healing as well. Metaphyseal sites generally heal faster than diaphyseal sites. The femur has been shown to heal faster than the tibia^28,141, and tibiae lengthened at two sites heal faster than those lengthened at only one site⁶³.

Other, less controllable factors also affect the rate of healing. Older patients tend to heal more slowly, with greater delays occurring after the age of twenty years^12,63. In a series of tibial lengthenings performed at one site in the bone, the healing index in children was 0.87 month per centimeter of new bone and that in adults was 1.5 months per centimeter¹². Several authors have found faster healing (and a lower healing index) in patients who have achondroplasia compared with patients who have another condition, such as congenital or post-traumatic limb-length discrepancy^24,37,146.

Certain congenital conditions, such as fibular hemimelia and proximal femoral focal deficiency in their severe forms, have traditionally necessitated amputation with early prosthetic fitting¹⁴⁴. Grill et al.⁷⁹, in a study of fifty-one patients who had severe forms of proximal femoral focal deficiency and an intact hip joint, reported lengthening of as much as sixteen centimeters. Catagni et al.⁴⁰ found that patients who had severe fibular hemimelia needed multiple staged lengthenings throughout childhood. Treatment included both femoral and tibial lengthening with eventual arthrodesis of the ankle by extension of the frame to the foot. Complications were numerous and included contracture of the knee, recurrent deformity of the foot, and one case of chronic edema. Although the Ilizarov method has clearly expanded the traditional indications and success rates for lengthening, it has not solved the problems posed by the most severe congenital deficiencies, for which amputation may still be the best option.

Lengthening of the forearm has been reported for a variety of indications, including radial hypoplasia²⁵, radiohumeral synostosis, ulnar dysplasia with a dislocated radial head, growth arrest, epiphyseal dysplasia, and Madelung deformity^{25,115,150,167}. In one series¹⁶⁷, thirteen forearms (in twelve patients) were lengthened by 10 to more than 100 per cent, but extensive splinting and therapy were needed to avoid contractures and a radial-nerve palsy developed in three patients. The length of the forearm of patients who have radial clubhand has been doubled without neural injury or permanent loss of function¹². The short ulna with radial deformity commonly seen with multiple osteochondromas has been treated more frequently with half-pin monolateral frames. In a series of seven patients who had this condition, pronation and supination were actually improved¹¹⁵.

The results of forty-three humeral lengthenings (of as much as sixteen centimeters from a corticotomy at the level of the deltoid tuberosity) were reported by Cattaneo et al.⁴⁴. The most common indications for the lengthening were achondroplasia and septic arthritis with proximal growth arrest. Although transient neurapraxia occurred in three patients, the long-term results were good.

Most of the literature on limb-lengthening to correct short stature has come from Europe, where a relative paucity of social adaptive mechanisms favors taller individuals. However, in the United States, such lengthening is controversial and not well accepted. The bulky limbs of achondroplastic dwarfs, with what appears to be a relative excess of muscle, permit massive lengthenings of bone with minimum contractures. Other disorders related to short stature, including endocrine and osteochondral dysplasias, have been treated with lengthening^137,146. Preoperative psychological testing¹⁰⁵ has been recommended to determine whether the patient and his or her support group have the emotional stability to undergo numerous operations and years of external fixation. Bilateral tibial, femoral, and humeral lengthening must be timed appropriately, staged, and integrated in the over-all plan of treatment^137,146,166. In one of the largest series of limb-lengthening procedures to treat achondroplasia¹⁶⁶, the tibiae and femora of 104 patients were lengthened as much as seventeen centimeters, for a total increase in standing height of as much as thirty-three centimeters.

Complications
Independent of the method used and the etiology of the problem to be treated, limb-lengthening is routinely associated with a plethora of complications. Complications can involve the pin tracks, bones, joints, neurovascular structures, and even mental status⁵⁸. Inflammation surrounding pin tracks is common as a result of mechanical or thermal damage, cellulitis, abscess, or local osteomyelitis. Osseous complications may involve premature or delayed consolidation, non-union, axial deviation, late bending, or fracture. During the lengthening, motion of the joint may be temporarily or permanently lost as a result of muscle contracture, arthrofibrosis, or damage to the cartilage. Nerves and vessels may be damaged directly by pins or osteotomes or indirectly by the actual stretching. Regional edema is common; painful neurapraxia is less common; and systemic hypertension, reflex sympathetic dystrophy, and compartment syndrome are rare⁵⁸.

Despite a decreased rate of complications^28,51,79,144 compared with the traditional Wagner technique⁸⁰, the Ilizarov method for limb-lengthening has led to higher rates of complications in the Western experience^52,127 than in the experience reported by Ilizarov himself. There is quite a disparity between the rates of complications reported by Wagner (twenty-six of fifty-eight patients; 45 per cent), DeBastiani (fourteen of 100; 14 per cent), and Ilizarov (twelve of 237; 5 per cent) with use of their respective techniques⁵², and there is an even greater disparity when the rates of complications in other series (as much as 225 per cent; 142 complications associated with sixty-three lengthenings) are compared^52,127.

Two independent reports revealed that the rate of major complications decreased substantially as the experience of the surgeon increased. In one study⁵², the over-all rate of complications was 72 per cent, but after thirty lengthening procedures the rate began to decrease (final rate, 25 per cent). In the other study¹⁶⁵, major complications followed eighteen (69 per cent) of twenty-six Ilizarov lengthenings performed in the first six months but only eight (35 per cent) of twenty-three lengthenings performed in the third six-month period of experience¹⁶⁵. In both studies, the rate of minor complications remained relatively constant, independent of the experience of the surgeon and the type of fixator^52,165.

Generally, the number of complications and failures of lengthenings increases in proportion to the length of the distraction^52,83,165. The number of complications is also associated with the severity of the preoperative problem but is not dependent on the type of external fixator⁵². The pain immediately after an Ilizarov procedure appears to be similar in magnitude to that after a standard osteotomy; however, some pain persists throughout the entire period of external fixation¹⁷⁹. The prevalence of inflammation at the pin sites has been reported to be as high as 95 per cent (ninety-five of 100 patients¹²); it usually resolves (rate of resolution, 97 per cent [ninety-two of ninety-five patients]¹²) with local pin care with or without oral administration of antibiotics for five days¹². Subluxation and contracture of the joint are two of the more serious complications. They can be minimized with preoperative planning, including protection against subluxation by spanning of the joint with the fixator, and with intensive therapy and splinting during the fixation period^48,74,90,159.

In an isolated case report, a fifteen-year-old boy had an osteosarcoma at the site of a femoral lengthening through an area of fibrous dysplasia four years after an Ilizarov procedure⁸⁵. Although spontaneous sarcomatous degeneration has been reported in regions of fibrous dysplasia⁸⁵, this case report raises the question of a possible association between the activation of new-bone formation in dysplastic bone and subsequent malignant degeneration.

Correction of Deformities and Non-Unions
Non-unions can be treated with the Ilizarov method with use of minimally invasive percutaneous techniques (Fig. 4-A). Bone and soft-tissue deformities can be corrected gradually in a single plane or in multiple planes, allowing for normalization of the mechanical axis. Articular deformities have been corrected by gradual stretching of soft tissues by means of transosseous external fixation with special distraction hinges to protect hyaline cartilage against excessive compression.

View larger version (30K): [in this window] [in a new window]   Fig. 4-A Lateral radiograph showing a combined hypertrophic (posterior) and atrophic (anterior) non-union of a left tibia with a fixed 61-degree anterior bow. The plantar flexors of the foot were contracted across the relatively shortened concave side of the deformity.

Deformities
The treatment of limb deformities requires meticulous analysis of the clinical and radiographic features to determine the true deformity. The Ilizarov method gives the surgeon the option of correcting osseous deformity and soft-tissue contracture acutely or gradually, or both. It has even been possible to correct deformities in certain types of pathologically involved bone⁶¹, including that seen in melorheostosis^23,117,155. The construction of the frame generally includes four-point fixation to obtain a mechanical advantage through fulcrum hinges and finely threaded inclined rods with a long lever arm to angulate, translate, rotate, or lengthen the bone segments gradually (Fig. 4-B). With accurate placement of the fulcrum hinges and stable fixation, the mechanical axis can be corrected gradually while bone formation and soft-tissue adaptation are facilitated. Because correction may not be possible at the true level of deformity, the anatomical axes cannot always be normalized; it may be necessary to create compensating deformities to correct the over-all mechanical axis of the limb.

View larger version (114K): [in this window] [in a new window]   Fig. 4-B Photograph of the frame in place. The frame appears complex but can be understood by visualizing the proximal and distal two-ring constructs connected by hinges (the medial hinge is visible) located at the central non-union to distract the posterior, hypertrophic non-union and to compress the anterior, atrophic non-union. A distraction rod is located posteriorly to push apart the ring constructs through the hinges, which act as a fulcrum to focus the forces at specific parts of the non-union. From the anterior plate attached to the rings, two threaded rods are connected to a dual half-ring construct with transosseous wires, which compress the non-union and deliver apical compression forces to the angular deformity. Stiff non-unions necessitate a strong frame such as this one to control the correction. The frame extends to the calcaneus to avoid equinus of the foot while the plantar flexors are gradually stretched by the frame.

Non-Unions
Ilizarov differentiated between hypertrophic and atrophic types of non-unions on the basis of clinical and radiographic findings to determine the treatment strategy that would facilitate healing, and he proposed specific methods of treatment for each type.

Hypertrophic non-unions have a vital blood supply from each bone end and a dense collagenous interface. For these reasons, bone formation can be stimulated by primary distraction^41,42 (Fig. 4-C). Catagni et al.⁴² used this strategy to treat twenty-one hypertrophic non-unions in nineteen patients. A stable union and correction of the deformities were achieved in all patients. Atrophic non-unions, with thin, non-reactive bone ends, are treated initially with compression and then with distraction. In one series¹³⁵, twenty-two atrophic tibial non-unions in patients who ranged in age from nineteen to sixty-two years were treated with this technique. The mean time to union was 13.6 months but included time for healing of additional sites of lengthening in many patients.

View larger version (83K): [in this window] [in a new window]   Fig. 4-C Lateral radiograph made after angular correction demonstrating spontaneous new-bone formation across the triangular opening wedge posteriorly to bridge the edges of the hypertrophic non-union. The anterior 25 per cent is not yet in contact beforre final compression.

Bone Transport
Intercalary defects resulting from trauma, infection, tumor, or prosthetic replacement can be treated with transport of a segment of bone within the limb⁹⁶. The method of bone transport is perhaps the most unique of Ilizarov's innovations. Major intercalary defects in bone have been bridged and new bone has formed in the defect with concomitant restoration of the osseous integrity and alignment of the limb. Bone grafts have not been necessary in many patients, and limb length has been regained. Chronic focal, segmental, and cavitary osteomyelitis have all been treated with bone transport: the osteomyelitic bone is excised, and generation of bone is induced in the resultant defect^10,43.

The bone segment must have an adequate blood supply to promote bone formation at its trailing end and healing at its leading end, which is compressed against the host bone^10,12,18. The ring fixator allows transport of bone segments in any direction with use of oblique pulling or transverse tensioned wires or half-pins^18,43,56,126.

Pulling, or oblique, wires tend to minimize scarring of the skin and interference with soft tissues, facilitating transports in long defects, where nerves or vessels may cross the path of transverse wires or half-pins^18,126. Pulling wires may be the only way to transport partial bone fragments in an oblique or transverse direction^10,43. Transverse wires or half-pins are used primarily for axial transport, preferably for shorter defects. They offer the advantage of transmitting more force to the soft tissues, which is helpful for closing soft-tissue defects^18,126. With axial bone transport, an intramedullary guide-wire or rod may be used without interfering with bone formation and healing as long as the periosteum is maintained^32,57. Multiple segments can be transported in the same or opposite directions to accelerate bone formation in the defect¹².

The basic principles of the Ilizarov method—stable fixation, a low-energy osteotomy with gradual distraction, and bone formation by intramembranous ossification—are the same for bone transport as for lengthening⁵⁶. As previously noted, although the classic Ilizarov method called for healing of the docking site by gradual and prolonged compression^43,96, Western surgeons have found that supplementation with autogenous bone graft after operative débridement of the ends of the bone accelerates and facilitates healing^46,76.

Bone transport has been successful in the treatment of infected non-unions^43,70,78. In a study by Cattaneo et al.⁴³, union was achieved in all thirteen patients in whom an infected non-union had been treated without the use of bone graft or a microvascular procedure. Several investigators have compared bone transport with the use of bone graft, antibiotic beads, and vascularized grafts for the treatment of segmental bone defects with or without infection^46,76,114. Most have reported similar rates of healing, durations of treatment, final angulations, numbers of complications, and total numbers of operative procedures among these treatment modalities; however, limb-length discrepancy was decreased with bone transport. The most commonly reported problems encountered with bone-grafting included limited availability of autogenous graft, donor-site morbidity, and fracture of the graft. With bone transport, nearly half of the patients needed supplemental bone-grafting of the docking site to facilitate healing. Joint contractures were also common. Cierny and Zorn⁴⁶ concluded that advantages of the Ilizarov method include fewer complications (seven [33 per cent] of twenty-one with bone transport compared with fourteen [61 per cent] of twenty-three with bone-grafting), decreased costs of treatment, and a shorter duration of disability (seventeen months compared with twenty-two months).

Bone transport has been successfully employed after a previous microvascular muscle flap transplantation¹⁶³ or with simultaneous use of antibiotic beads³⁵. Bone transport can also be used to treat congenital pseudarthrosis of the tibia, a condition that has remained refractory to most conventional methods of bone-grafting. The procedure necessitates open resection of the pseudarthrosis and intramedullary fixation^60,134. Paley et al.¹³⁴ used this method to treat congenital tibial pseudarthrosis in sixteen patients. The deformity was corrected in all patients, and fifteen of the sixteen had a union at the four-year follow-up examination¹³⁴.

Treatment of Fractures
The Ilizarov method offers an alternative to conventional treatment of high-energy fractures of the tibia^110,162. In one study, forty-one unstable tibial fractures with substantial loss of bone were treated with simultaneous compression of the fracture site and adjacent lengthening of the affected bone¹⁶². All of the fractures healed without bone-grafting, with the time to union ranging from twelve to forty-seven weeks (mean, 25.6 weeks).

Small-wire external fixation for treatment of high-energy fractures of the tibial plateau offers several advantages. Percutaneous placement of the wire minimizes additional devitalization of small bone fragments, and beaded wires can be used to reduce and compress condylar fractures. The circular frame allows stabilization of the periarticular segment, promoting early motion and weight-bearing. Areas of segmental bone loss can be stabilized, with regeneration induced later with the Ilizarov method. Rotational, translational, and angular malalignments can be corrected during the healing process if they are not reduced initially. Watson¹⁷² reported that thirty-one Schatzker type-VI injuries of the tibial plateau that had been treated with circular external fixation all demonstrated radiographic healing, at a mean of fifteen weeks and with a mean range of motion of the knee of 106 degrees.

	Operative Procedures under Development

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The Ilizarov method has been used for reconstruction of the feet with a variety of conditions^{33,53,71,86,98,128}. Stiffness of the foot is a common result of such treatment. Therefore, an important prerequisite for this operation is a stiff foot with secondary problems such as deformity, pain, non-union, and shortening. Amputation should be discussed as an option.

Arthrodiastasis, the use of a distraction hinge to stretch periarticular soft tissues while protecting underlying cartilage or even allowing fibrocartilage to fill a narrowed joint space, is a unique variation of the Ilizarov method¹⁰⁹. Flexion contractures of the knee^81,89 and elbow¹¹⁹ and stiffness of the hip^3,38 have been treated, with mixed results.

The correction of spinal deformities has been attempted^26,72. Mandibular lengthening^50,66,101 has attracted the interest of craniofacial surgeons. Lengthening of the stump, especially in the upper extremity, has facilitated the use of prostheses^150,157. Soft-tissue distraction has been used to create a soft-tissue envelope with intact host vessels for a subsequent vascularized fibular transplant⁹⁹. The Ilizarov method has been used as a limb-salvage procedure after resection of malignant tumors³⁹. Indications have included failure of an allograft or progressive limb-length discrepancy.

	Costs

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The decreased rates of complications, decreased operative durations, and shorter inpatient stays associated with the Ilizarov method contributed to savings of approximately $30,000 per patient compared with conventional methods of limb salvage (such as sequestrectomy, antibiotic beads, free flaps, and bone-grafting) in one study⁴⁶. The cost of major limb salvage with the Ilizarov method was also compared with that of amputation¹⁷⁵. While the cost of the acute care necessitated by the amputation was much lower, the projected costs of prosthetic care for the remainder of the patient's life resulted in greater over-all cost.

	Future Directions

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Ilizarov died in 1992; however, his method is currently used to treat a spectrum of conditions. Basic research on the bone formation seen with the Ilizarov method has led to greater understanding of the biology of bone formation in general. Current research focuses on methods to accelerate bone formation, promote muscle growth, and avoid transcutaneous fixation. Since intramedullary rods have been shown to be compatible with bone formation²⁹, work is underway to develop an expanding intramedullary rod that avoids the use of external fixation pins. Other areas of ongoing research include the application of distraction forces at different rates to regenerate cruciate ligaments²². Ongoing biological research, technological innovations, and careful clinical trials will perpetuate Ilizarov's contributions to the treatment of severe musculoskeletal conditions.

	Footnotes

 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.

Arkansas Children's Hospital, 800 Marshall Street, Little Rock, Arkansas 72205-3591.

	References

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